TY - JOUR
T1 - Imaging the snorkel effect during submerged germination in rice
T2 - Oxygen supply via the coleoptile triggers seminal root emergence underwater
AU - Shiono, Katsuhiro
AU - Koshide, Akiko
AU - Iwasaki, Kazunari
AU - Oguri, Kazumasa
AU - Fukao, Takeshi
AU - Larsen, Morten
AU - Glud, Ronnie N.
N1 - Funding Information:
This work was partly supported by JSPS KAKENHI (grant nos. JP16KK0173, JP19K05978, JP22K05587, and JP22H02322 to KS and JP20H02013 to RG). Additional support was provided by HADES-ERC Advanced Grant (grant no. 669947 to RG), the Danish National Research Foundation through the Danish Center for Hadal Research, HADAL (grant no. DNRF145 to RG), and the Strategic Research Promotion Grant from Fukui Prefectural University (to KS).
Publisher Copyright:
Copyright © 2022 Shiono, Koshide, Iwasaki, Oguri, Fukao, Larsen and Glud.
PY - 2022/7/29
Y1 - 2022/7/29
N2 - 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 (O2) to initiate the first leaf elongation and seminal root emergence. Here, we obtained direct evidence for this hypothesis by visualizing the spatiotemporal O2 dynamics during submerged germination in rice using a planar O2 optode system. In parallel with the O2 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, O2 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 O2, seminal roots emerged. A transient O2 burst around the embryo was shown to be essential for seminal root emergence during submerged rice germination. The parallel application of a planar O2 optode system and automated scanning system can be a powerful tool for examining how environmental conditions affect germination in rice and other plants.
AB - 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 (O2) to initiate the first leaf elongation and seminal root emergence. Here, we obtained direct evidence for this hypothesis by visualizing the spatiotemporal O2 dynamics during submerged germination in rice using a planar O2 optode system. In parallel with the O2 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, O2 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 O2, seminal roots emerged. A transient O2 burst around the embryo was shown to be essential for seminal root emergence during submerged rice germination. The parallel application of a planar O2 optode system and automated scanning system can be a powerful tool for examining how environmental conditions affect germination in rice and other plants.
KW - anoxia
KW - flatbed scanning system
KW - hypoxia
KW - Oryza sativa
KW - oxygen imaging
KW - planar oxygen optode
KW - seminal root development
KW - spatiotemporal imaging
U2 - 10.3389/fpls.2022.946776
DO - 10.3389/fpls.2022.946776
M3 - Journal article
C2 - 35968087
AN - SCOPUS:85135883751
VL - 13
JO - Frontiers in Plant Science
JF - Frontiers in Plant Science
SN - 1664-462X
M1 - 946776
ER -