Oxygen Deprivation and Flooding HORT 301 – Plant Physiology November 16, 2009 Taiz and Zeiger – Chapter 11 (p ), Chapter 26 (p ); Bray et al., Chapter 22, and Bailey-Serres and Voesenek (2008) Annu Rev Plant Biol Flooding causes no (anoxia) or low (hypoxia) O 2 Insufficient O 2 availability inhibits respiration and ATP production ADD FIGURE 7-55 FROM SMITH ET AL.

Courtesy of Bob Joly Flooding reduces gas exchange between plant cells and the atmosphere Reduced O 2 and increased CO 2 and ethylene in cells

Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants Insufficient gas exchange negatively affects ATP production and other physiological processes Low O 2 reduces TCA cycle activity, inhibition of ATP production Oxidative phosphorylation requires O 2 for electron transport (electron acceptor) Reduced NADH oxidation and NAD + is limiting for glycolysis Glucose + 2NAD + + 2ADP + 2Pi → 2 pyruvate + 2NADH + 2H + + 2ATP + 2H 2 O Flooding of the Midwest (1993) resulted in a 33% reduction in maize yield

Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants Cells initiate fermentative metabolism that oxidizes NADH to NAD + Two (2) ATP molecules produced per hexose molecule through fermentation Reduced pH causes ethanol production

Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants Anaerobic environment in the soil results in production of toxins Reduced root function that causes wilting Ethylene is induced by low O 2 and leads to epinasty

Hypoxia and anoxia result in these detrimental effects: Low oxygen reduces TCA cycle activity NADH oxidation (to NAD + ) is limited ATP production per hexose is reduced from 30/32 to 2 (fermentation cycle to convert NADH to NAD + ) Reduced intracellular pH leading to cell death Anaerobic microbes in the soil reduce ions to toxic forms Ethylene production results in epinasty

Adaptation and acclimation responses that increase low O 2 tolerance Plants complete life cycle during periods when flooding does not occur Quiescence during flooding, high fermentative capacity Quiescence Intolerant Acclimation

Bailey-Serres & Voesenek (2008) Annu Rev Plant Biol Low O 2 escape syndromes(LOES) that mitigate hypoxia: Increased elongation of stems, petioles and leaves facilitates contact with air Thinner leaf blades (cell wall and cuticle thickness) and orientation of chloroplasts to leaf surface facilitate O 2 diffusion into the leaf

Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants Aerenchyma creates internal air spaces in root cortical region to facilitate O 2 diffusion Aerenchyma may occur innately (rice) or be induced (maize) Maize

Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants Low O 2 induces ethylene production that leads to aerenchyma formation

Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants Adventitious root and lenticel formation in response to flooding

Smith et al. (2010) Plant Biology.

Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants Deepwater rice acclimates to flooding Rapid shoot intermodal elongation to access O 2 during flooding Development of adventitious roots post-flood for propagation

Lowland RiceDeepwater Rice TolerantIntolerant Strategy QuiescenceLOES Sub1 haplotype SUB1A-1, SUB1B, SUB1C SUB1B, SUB1C or SUB1A-2, SUB1B, SUSB1C SUB1B, SUB1C or SUB1A-2, SUB1B, SUB1C Carbohydrate consumption Limited by SUB1A-1 High Fermentation capacity HighModerateN.D. GA response Inhibited by SUB1A-1 Promoted by SUB1C High Bailey-Serres & Voesenek (2008) Annu Rev Plant Biol Intolerant and tolerant rice varieties respond to flooding by different mechanisms

Low O 2 sensing is proposed to regulate acclimation responses Fermentation and combined reduced growth is acclimation strategy Low O 2 sensor (receptor) → reactive oxygen species → Ca 2+ transients → induction of fermentation enzymes Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants

Bailey-Serres & Voesenek (2008) Annu Rev Plant Biol Low O 2 induces ethylene biosynthetic genes and is the initial signal leading to shoot and leaf elongation Ethylene down-regulates ABA levels by reducing NCED expression which promotes GA function

Low O 2 regulates gene expression at the transcriptional and post- transcriptional levels

Hypoxia acclimates plants to tolerate anoxia