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Morphological Characterization and Transcriptional Regulation of Corolla Closure in Ipomoea purpurea

Corolla closure protects pollen from high-temperature stress during pollen germination and fertilization in the ornamental plant morning glory (Ipomoea purpurea). However, the morphological nature of this process and the molecular events underpinning it remain largely unclear. Here, we examined the...

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Autores principales: Zhang, Peipei, Sun, Mingyue, Wang, Xiaoqiong, Guo, Runjiu, Sun, Yuchu, Gui, Mengyuan, Li, Jingyuan, Wang, Taixia, Zhang, Liang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8453026/
https://www.ncbi.nlm.nih.gov/pubmed/34557209
http://dx.doi.org/10.3389/fpls.2021.697764
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author Zhang, Peipei
Sun, Mingyue
Wang, Xiaoqiong
Guo, Runjiu
Sun, Yuchu
Gui, Mengyuan
Li, Jingyuan
Wang, Taixia
Zhang, Liang
author_facet Zhang, Peipei
Sun, Mingyue
Wang, Xiaoqiong
Guo, Runjiu
Sun, Yuchu
Gui, Mengyuan
Li, Jingyuan
Wang, Taixia
Zhang, Liang
author_sort Zhang, Peipei
collection PubMed
description Corolla closure protects pollen from high-temperature stress during pollen germination and fertilization in the ornamental plant morning glory (Ipomoea purpurea). However, the morphological nature of this process and the molecular events underpinning it remain largely unclear. Here, we examined the cellular and gene expression changes that occur during corolla closure in the I. purpurea. We divided the corolla closure process into eight stages (S0–S7) based on corolla morphology. During flower opening, bulliform cells appear papillate, with pigments in the adaxial epidermis of the corolla. These cells have distinct morphology from the smaller, flat cells in the abaxial epidermis in the corolla limb and intermediate of the corolla. During corolla closure, the bulliform cells of the adaxial epidermis severely collapse compared to cells on the abaxial side. Analysis of transparent tissue and cross sections revealed that acuminate veins in the corolla are composed of spiral vessels that begin to curve during corolla closure. When the acuminate veins were compromised, the corolla failed to close normally. We performed transcriptome analysis to obtain a time-course profile of gene expression during the process from the open corolla stage (S0) to semi-closure (S3). Genes that were upregulated from S0 to S1 were enriched in the polysaccharide degradation pathway, which positively regulates cell wall reorganization. Senescence-related transcription factor genes were expressed beginning at S1, leading to the activation of downstream autophagy-related genes at S2. Genes associated with peroxisomes and ubiquitin-mediated proteolysis were upregulated at S3 to enhance reactive oxygen species scavenging and protein degradation. Therefore, bulliform cells and acuminate veins play essential roles in corolla closure. Our findings provide a global understanding of the gene regulatory processes that occur during corolla closure in I. purpurea.
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spelling pubmed-84530262021-09-22 Morphological Characterization and Transcriptional Regulation of Corolla Closure in Ipomoea purpurea Zhang, Peipei Sun, Mingyue Wang, Xiaoqiong Guo, Runjiu Sun, Yuchu Gui, Mengyuan Li, Jingyuan Wang, Taixia Zhang, Liang Front Plant Sci Plant Science Corolla closure protects pollen from high-temperature stress during pollen germination and fertilization in the ornamental plant morning glory (Ipomoea purpurea). However, the morphological nature of this process and the molecular events underpinning it remain largely unclear. Here, we examined the cellular and gene expression changes that occur during corolla closure in the I. purpurea. We divided the corolla closure process into eight stages (S0–S7) based on corolla morphology. During flower opening, bulliform cells appear papillate, with pigments in the adaxial epidermis of the corolla. These cells have distinct morphology from the smaller, flat cells in the abaxial epidermis in the corolla limb and intermediate of the corolla. During corolla closure, the bulliform cells of the adaxial epidermis severely collapse compared to cells on the abaxial side. Analysis of transparent tissue and cross sections revealed that acuminate veins in the corolla are composed of spiral vessels that begin to curve during corolla closure. When the acuminate veins were compromised, the corolla failed to close normally. We performed transcriptome analysis to obtain a time-course profile of gene expression during the process from the open corolla stage (S0) to semi-closure (S3). Genes that were upregulated from S0 to S1 were enriched in the polysaccharide degradation pathway, which positively regulates cell wall reorganization. Senescence-related transcription factor genes were expressed beginning at S1, leading to the activation of downstream autophagy-related genes at S2. Genes associated with peroxisomes and ubiquitin-mediated proteolysis were upregulated at S3 to enhance reactive oxygen species scavenging and protein degradation. Therefore, bulliform cells and acuminate veins play essential roles in corolla closure. Our findings provide a global understanding of the gene regulatory processes that occur during corolla closure in I. purpurea. Frontiers Media S.A. 2021-09-07 /pmc/articles/PMC8453026/ /pubmed/34557209 http://dx.doi.org/10.3389/fpls.2021.697764 Text en Copyright © 2021 Zhang, Sun, Wang, Guo, Sun, Gui, Li, Wang and Zhang. https://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
Zhang, Peipei
Sun, Mingyue
Wang, Xiaoqiong
Guo, Runjiu
Sun, Yuchu
Gui, Mengyuan
Li, Jingyuan
Wang, Taixia
Zhang, Liang
Morphological Characterization and Transcriptional Regulation of Corolla Closure in Ipomoea purpurea
title Morphological Characterization and Transcriptional Regulation of Corolla Closure in Ipomoea purpurea
title_full Morphological Characterization and Transcriptional Regulation of Corolla Closure in Ipomoea purpurea
title_fullStr Morphological Characterization and Transcriptional Regulation of Corolla Closure in Ipomoea purpurea
title_full_unstemmed Morphological Characterization and Transcriptional Regulation of Corolla Closure in Ipomoea purpurea
title_short Morphological Characterization and Transcriptional Regulation of Corolla Closure in Ipomoea purpurea
title_sort morphological characterization and transcriptional regulation of corolla closure in ipomoea purpurea
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8453026/
https://www.ncbi.nlm.nih.gov/pubmed/34557209
http://dx.doi.org/10.3389/fpls.2021.697764
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