#34 Flooding and Oxygen Deprivation HORT 301 – Plant Physiology November 19, 2010 Taiz and Zeiger – Chapter 11 (p ), Chapter 26 (p ) Bailey-Serres and Voesenek (2008) Annu Rev Plant Biol Flooding causes no (anoxia) or low (hypoxia) O 2 Okefenokee Swamp, GeorgiaGreat Dismal Swamp, North Carolina 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 2

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 3

Smith et al. (2010) Plant Biology. Anaerobic metabolism Fermentation 4

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, 30 to 32 via respiration Reduced pH causes ethanol production 5

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 Soil microbes reduce NO 3 - to NO 2 - /N 2 O, Fe 3+ to Fe 2+, SO 4 2- to H 2 S 6

Hypoxia and anoxia result in these detrimental effects: Low oxygen reduces TCA cycle activity, which reduces availability of NAD + for glycolysis ATP production per hexose is reduced from 30/32 to 2 (fermentation cycle to convert NADH to NAD + ) Reduced intracellular pH may cause cell death Anaerobic microbes in the soil reduce ions to toxic forms, reducing root function 7

Adaptation and acclimation responses that increase low O 2 tolerance Plants complete life cycle during periods when flooding does not occur Morphological adaptation or acclimation WillowMangrove Smith et al. (2010) Plant Biology 8

Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants Adventitious root and lenticel formation induced as a response to flooding 9

Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants Aerenchyma are internal air spaces in root cortical region that facilitate O 2 diffusion Aerenchyma may occur innately (rice) or be induced (maize) Maize 10

Smith et al. (2010) Plant Biology. Aerenchyma formation in maize roots 11

Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants Low O 2 induces ethylene production that leads to aerenchyma formation 12

Rice responses to low O 2 Quiescence (lowland) Intolerant Escape (deep water) 13

Bailey-Serres & Voesenek (2008) Annu Rev Plant Biol Low O 2 escape syndrome that mitigates hypoxia Increased elongation of stems, petioles and leaves facilitates contact with air Aerenchyma and thinner leaf blades (cell wall and cuticle thickness) and orientation of chloroplasts to leaf surface facilitate O 2 diffusion into the leaf 14

Hattori et al (2009) Nature 460: Submergence escape – SNORKEL1 (SK1) and SNORKEL2 (SK2) 15

Fukao et al (2008) Annals of Botany 103:143 Low oxygen quiescence – SUBMERGENCE1A-1 (SUB1A-1) 16

Xu et al (2006) Nature 442:705 SUB1 introgression by maker assisted selection 17

18 SUB1A-1 and submergence tolerance

Voesenek and Bailey-Serres (2009) Nature 460: Escape and quiescence strategies for flooding tolerance 19

Low O 2 or ROS sensing may regulate submergence responses Low O 2 sensor (receptor) → reactive oxygen species → Ca 2+ transients → induction of fermentation enzymes Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants 20

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 21

Low O 2 regulates gene expression at the transcriptional and post- transcriptional levels Bray et al. (2000) 22

Hypoxia acclimates plants to tolerate anoxia Buchanan et al. (2000) (Biochemistry & Molecular Biology of Plants 23

24 SUB1A-1 and submergence tolerance