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Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater

Submergence during germination impedes aerobic metabolisms and limits the growth of most higher plants. However, some wetland plants including rice can germinate under submerged conditions. It has long been hypothesized that the first elongating shoot tissue, the coleoptile, acts as a snorkel to acq...

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Autores principales: Shiono, Katsuhiro, Koshide, Akiko, Iwasaki, Kazunari, Oguri, Kazumasa, Fukao, Takeshi, Larsen, Morten, Glud, Ronnie N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9372499/
https://www.ncbi.nlm.nih.gov/pubmed/35968087
http://dx.doi.org/10.3389/fpls.2022.946776
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author Shiono, Katsuhiro
Koshide, Akiko
Iwasaki, Kazunari
Oguri, Kazumasa
Fukao, Takeshi
Larsen, Morten
Glud, Ronnie N.
author_facet Shiono, Katsuhiro
Koshide, Akiko
Iwasaki, Kazunari
Oguri, Kazumasa
Fukao, Takeshi
Larsen, Morten
Glud, Ronnie N.
author_sort Shiono, Katsuhiro
collection PubMed
description Submergence during germination impedes aerobic metabolisms and limits the growth of most higher plants. However, some wetland plants including rice can germinate under submerged conditions. It has long been hypothesized that the first elongating shoot tissue, the coleoptile, acts as a snorkel to acquire atmospheric oxygen (O(2)) to initiate the first leaf elongation and seminal root emergence. Here, we obtained direct evidence for this hypothesis by visualizing the spatiotemporal O(2) dynamics during submerged germination in rice using a planar O(2) optode system. In parallel with the O(2) imaging, we tracked the anatomical development of shoot and root tissues in real-time using an automated flatbed scanner. Three hours after the coleoptile tip reached the water surface, O(2) levels around the embryo transiently increased. At this time, the activity of alcohol dehydrogenase (ADH), an enzyme critical for anaerobic metabolism, was significantly reduced, and the coleorhiza covering the seminal roots in the embryo was broken. Approximately 10 h after the transient burst in O(2), seminal roots emerged. A transient O(2) burst around the embryo was shown to be essential for seminal root emergence during submerged rice germination. The parallel application of a planar O(2) optode system and automated scanning system can be a powerful tool for examining how environmental conditions affect germination in rice and other plants.
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spelling pubmed-93724992022-08-13 Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater Shiono, Katsuhiro Koshide, Akiko Iwasaki, Kazunari Oguri, Kazumasa Fukao, Takeshi Larsen, Morten Glud, Ronnie N. Front Plant Sci Plant Science Submergence during germination impedes aerobic metabolisms and limits the growth of most higher plants. However, some wetland plants including rice can germinate under submerged conditions. It has long been hypothesized that the first elongating shoot tissue, the coleoptile, acts as a snorkel to acquire atmospheric oxygen (O(2)) to initiate the first leaf elongation and seminal root emergence. Here, we obtained direct evidence for this hypothesis by visualizing the spatiotemporal O(2) dynamics during submerged germination in rice using a planar O(2) optode system. In parallel with the O(2) imaging, we tracked the anatomical development of shoot and root tissues in real-time using an automated flatbed scanner. Three hours after the coleoptile tip reached the water surface, O(2) levels around the embryo transiently increased. At this time, the activity of alcohol dehydrogenase (ADH), an enzyme critical for anaerobic metabolism, was significantly reduced, and the coleorhiza covering the seminal roots in the embryo was broken. Approximately 10 h after the transient burst in O(2), seminal roots emerged. A transient O(2) burst around the embryo was shown to be essential for seminal root emergence during submerged rice germination. The parallel application of a planar O(2) optode system and automated scanning system can be a powerful tool for examining how environmental conditions affect germination in rice and other plants. Frontiers Media S.A. 2022-07-29 /pmc/articles/PMC9372499/ /pubmed/35968087 http://dx.doi.org/10.3389/fpls.2022.946776 Text en Copyright © 2022 Shiono, Koshide, Iwasaki, Oguri, Fukao, Larsen and Glud. 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
Shiono, Katsuhiro
Koshide, Akiko
Iwasaki, Kazunari
Oguri, Kazumasa
Fukao, Takeshi
Larsen, Morten
Glud, Ronnie N.
Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater
title Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater
title_full Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater
title_fullStr Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater
title_full_unstemmed Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater
title_short Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater
title_sort imaging the snorkel effect during submerged germination in rice: oxygen supply via the coleoptile triggers seminal root emergence underwater
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9372499/
https://www.ncbi.nlm.nih.gov/pubmed/35968087
http://dx.doi.org/10.3389/fpls.2022.946776
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