Energetics of acclimation to NaCl by submerged, anoxic rice seedlings

Budiastuti Kurniasih, Hank Greenway, Timothy David Colmer

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Background and aims: Our aim was to elucidate how plant tissues under a severe energy crisis cope with imposition of high NaCl, which greatly increases ion fluxes and hence energy demands. The energy requirements for ion regulation during combined salinity and anoxia were assessed to gain insights into ion transport processes in the anoxia-tolerant coleoptile of rice. • Methods: We studied the combined effects of anoxia plus 50 or 100 mM NaCl on tissue ions and growth of submerged rice (Oryza sativa) seedlings. Excised coleoptiles allowed measurements in aerated or anoxic conditions of ion net fluxes and O2 consumption or ethanol formation and by inference energy production. • Key Results: Over 80 h of anoxia, coleoptiles of submerged intact seedlings grew at 100 mM NaCl, but excised coleoptiles, with 50 mM exogenous glucose, survived only at 50 mM NaCl, possibly due to lower energy production with glucose than for intact coleoptiles with sucrose as substrate. Rates of net uptake of Na+ and Cl- by coleoptiles in anoxia were about half those in aerated solution. Ethanol formation in anoxia and O2 uptake in aerobic solution were each increased by 13-15 % at 50 mM NaCl, i.e. ATP formation was stimulated. For acclimation to 50 mM NaCl, the anoxic tissues used only 25 % of the energy that was expended by aerobic tissues. Following return of coleoptiles to aerated non-saline solution, rates of net K+ uptake recovered to those in continuously aerated solution, demonstrating there was little injury during anoxia with 50 mM NaCl. • Conclusion: Rice seedlings survive anoxia, without the coleoptile incurring significant injury, even with the additional energy demands imposed by NaCl (100 mM when intact, 50 mM when excised). Energy savings were achieved in saline anoxia by less coleoptile growth, reduced ion fluxes as compared to aerobic coleoptiles and apparent energy-economic ion transport systems.

Original languageEnglish
Pages (from-to)129-142
Number of pages14
JournalAnnals of Botany
Volume119
Issue number1
DOIs
Publication statusPublished - 2017

Fingerprint

coleoptiles
acclimation
hypoxia
rice
seedlings
energy
ions
ion transport
uptake mechanisms
ethanol
glucose
energy requirements
anaerobic conditions
plant tissues
Oryza sativa
sucrose
salinity
economics

Cite this

Kurniasih, Budiastuti ; Greenway, Hank ; Colmer, Timothy David. / Energetics of acclimation to NaCl by submerged, anoxic rice seedlings. In: Annals of Botany. 2017 ; Vol. 119, No. 1. pp. 129-142.
@article{62a263fcbadd4baebf52c58d8cf4031e,
title = "Energetics of acclimation to NaCl by submerged, anoxic rice seedlings",
abstract = "Background and aims: Our aim was to elucidate how plant tissues under a severe energy crisis cope with imposition of high NaCl, which greatly increases ion fluxes and hence energy demands. The energy requirements for ion regulation during combined salinity and anoxia were assessed to gain insights into ion transport processes in the anoxia-tolerant coleoptile of rice. • Methods: We studied the combined effects of anoxia plus 50 or 100 mM NaCl on tissue ions and growth of submerged rice (Oryza sativa) seedlings. Excised coleoptiles allowed measurements in aerated or anoxic conditions of ion net fluxes and O2 consumption or ethanol formation and by inference energy production. • Key Results: Over 80 h of anoxia, coleoptiles of submerged intact seedlings grew at 100 mM NaCl, but excised coleoptiles, with 50 mM exogenous glucose, survived only at 50 mM NaCl, possibly due to lower energy production with glucose than for intact coleoptiles with sucrose as substrate. Rates of net uptake of Na+ and Cl- by coleoptiles in anoxia were about half those in aerated solution. Ethanol formation in anoxia and O2 uptake in aerobic solution were each increased by 13-15 {\%} at 50 mM NaCl, i.e. ATP formation was stimulated. For acclimation to 50 mM NaCl, the anoxic tissues used only 25 {\%} of the energy that was expended by aerobic tissues. Following return of coleoptiles to aerated non-saline solution, rates of net K+ uptake recovered to those in continuously aerated solution, demonstrating there was little injury during anoxia with 50 mM NaCl. • Conclusion: Rice seedlings survive anoxia, without the coleoptile incurring significant injury, even with the additional energy demands imposed by NaCl (100 mM when intact, 50 mM when excised). Energy savings were achieved in saline anoxia by less coleoptile growth, reduced ion fluxes as compared to aerobic coleoptiles and apparent energy-economic ion transport systems.",
keywords = "Anaerobic catabolism, Anoxia plus NaCl, Anoxia tolerance, Coleoptile, Complete submergence, Energetics, Energy crisis, Energy efficient transport, Ethanolic fermentation, Germination, NaCl x anoxia interaction, Oryza sativa, Salinity tolerance",
author = "Budiastuti Kurniasih and Hank Greenway and Colmer, {Timothy David}",
year = "2017",
doi = "10.1093/aob/mcw189",
language = "English",
volume = "119",
pages = "129--142",
journal = "Annals of Botany",
issn = "0305-7364",
publisher = "OXFORD UNIV PRESS UNITED KINGDOM",
number = "1",

}

Energetics of acclimation to NaCl by submerged, anoxic rice seedlings. / Kurniasih, Budiastuti; Greenway, Hank; Colmer, Timothy David.

In: Annals of Botany, Vol. 119, No. 1, 2017, p. 129-142.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Energetics of acclimation to NaCl by submerged, anoxic rice seedlings

AU - Kurniasih, Budiastuti

AU - Greenway, Hank

AU - Colmer, Timothy David

PY - 2017

Y1 - 2017

N2 - Background and aims: Our aim was to elucidate how plant tissues under a severe energy crisis cope with imposition of high NaCl, which greatly increases ion fluxes and hence energy demands. The energy requirements for ion regulation during combined salinity and anoxia were assessed to gain insights into ion transport processes in the anoxia-tolerant coleoptile of rice. • Methods: We studied the combined effects of anoxia plus 50 or 100 mM NaCl on tissue ions and growth of submerged rice (Oryza sativa) seedlings. Excised coleoptiles allowed measurements in aerated or anoxic conditions of ion net fluxes and O2 consumption or ethanol formation and by inference energy production. • Key Results: Over 80 h of anoxia, coleoptiles of submerged intact seedlings grew at 100 mM NaCl, but excised coleoptiles, with 50 mM exogenous glucose, survived only at 50 mM NaCl, possibly due to lower energy production with glucose than for intact coleoptiles with sucrose as substrate. Rates of net uptake of Na+ and Cl- by coleoptiles in anoxia were about half those in aerated solution. Ethanol formation in anoxia and O2 uptake in aerobic solution were each increased by 13-15 % at 50 mM NaCl, i.e. ATP formation was stimulated. For acclimation to 50 mM NaCl, the anoxic tissues used only 25 % of the energy that was expended by aerobic tissues. Following return of coleoptiles to aerated non-saline solution, rates of net K+ uptake recovered to those in continuously aerated solution, demonstrating there was little injury during anoxia with 50 mM NaCl. • Conclusion: Rice seedlings survive anoxia, without the coleoptile incurring significant injury, even with the additional energy demands imposed by NaCl (100 mM when intact, 50 mM when excised). Energy savings were achieved in saline anoxia by less coleoptile growth, reduced ion fluxes as compared to aerobic coleoptiles and apparent energy-economic ion transport systems.

AB - Background and aims: Our aim was to elucidate how plant tissues under a severe energy crisis cope with imposition of high NaCl, which greatly increases ion fluxes and hence energy demands. The energy requirements for ion regulation during combined salinity and anoxia were assessed to gain insights into ion transport processes in the anoxia-tolerant coleoptile of rice. • Methods: We studied the combined effects of anoxia plus 50 or 100 mM NaCl on tissue ions and growth of submerged rice (Oryza sativa) seedlings. Excised coleoptiles allowed measurements in aerated or anoxic conditions of ion net fluxes and O2 consumption or ethanol formation and by inference energy production. • Key Results: Over 80 h of anoxia, coleoptiles of submerged intact seedlings grew at 100 mM NaCl, but excised coleoptiles, with 50 mM exogenous glucose, survived only at 50 mM NaCl, possibly due to lower energy production with glucose than for intact coleoptiles with sucrose as substrate. Rates of net uptake of Na+ and Cl- by coleoptiles in anoxia were about half those in aerated solution. Ethanol formation in anoxia and O2 uptake in aerobic solution were each increased by 13-15 % at 50 mM NaCl, i.e. ATP formation was stimulated. For acclimation to 50 mM NaCl, the anoxic tissues used only 25 % of the energy that was expended by aerobic tissues. Following return of coleoptiles to aerated non-saline solution, rates of net K+ uptake recovered to those in continuously aerated solution, demonstrating there was little injury during anoxia with 50 mM NaCl. • Conclusion: Rice seedlings survive anoxia, without the coleoptile incurring significant injury, even with the additional energy demands imposed by NaCl (100 mM when intact, 50 mM when excised). Energy savings were achieved in saline anoxia by less coleoptile growth, reduced ion fluxes as compared to aerobic coleoptiles and apparent energy-economic ion transport systems.

KW - Anaerobic catabolism

KW - Anoxia plus NaCl

KW - Anoxia tolerance

KW - Coleoptile

KW - Complete submergence

KW - Energetics

KW - Energy crisis

KW - Energy efficient transport

KW - Ethanolic fermentation

KW - Germination

KW - NaCl x anoxia interaction

KW - Oryza sativa

KW - Salinity tolerance

UR - http://www.scopus.com/inward/record.url?scp=85014837061&partnerID=8YFLogxK

U2 - 10.1093/aob/mcw189

DO - 10.1093/aob/mcw189

M3 - Article

VL - 119

SP - 129

EP - 142

JO - Annals of Botany

JF - Annals of Botany

SN - 0305-7364

IS - 1

ER -