1

Biogeochemistry of WetlandsS i d A li tiS i d A li ti

Institute of Food and Agricultural Sciences (IFAS)

Science and ApplicationsScience and Applications

Wetland Biogeochemistry LaboratorySoil and Water Science Department

Adaptations of Plants to Anaerobiosis

6/22/2008 WBL 16/22/2008 16/22/2008 WBL 1

InstructorMark Clark

Clarkmw@ufl.edu

Soil and Water Science DepartmentUniversity of Florida

Adaptations of Plants to Soil AnaerobiosisAdaptations of Plants to Soil Anaerobiosis

Topic Outline

Role of oxygen in the plant

Potential stresses due to lack of oxygen

Physiological and morphological adaptations

Gas transport processes

6/22/2008 WBL 2

Oxidation of the rhizosphere

Flux of reduced gases

2

Learning Objectives

Adaptations of Plants to Soil AnaerobiosisAdaptations of Plants to Soil Anaerobiosis

Understand impacts of hypoxia and anoxia on plants.

Understand physiological and morphological adaptations that wetland plants have to overcome or minimize stress.

Learn about passive gas exchange processes that occur in wetlands vegetation.

6/22/2008 WBL 3

Understand what an oxidized rhizosphere is and what implications it has for the plant and soil biogeochemistry.

Realize that gas transport is a bidirectional pathway.

Plants and Al

Water Air

OXYGEN: Sources and SinksOXYGEN: Sources and Sinks

Soil OxygenSoil OxygenSoil OxygenSoil Oxygen

Algae Release byPlant Roots

Oxidation ofOxidation of Reductants

Respiration

Chemolithotrophicoxidation

Chemicaloxidation

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Do wetland plants require ?

Do wetland plants require ?oxygen?oxygen?

Do all plant organs require oxygen?

Do all plant organs require oxygen?oxygen?oxygen?

Drained SoilDrained Soil

Gas Exchange in Soil / Water / Plant System

Flooded SoilFlooded Soil

OO22

OO22

COCO22CO2, CH4, andother gases

Dissloved metalssulfides, and organic acids

?

4

Glucose Absence of Oxygen

Presence of Oxygen

Glucose MetabolismGlucose Metabolism

Pyruvate

Acetyl-CoAAcetate

Acetyl-CoA

Lactate

32 ATP32 ATP 2 ATP2 ATP

Electron transport chain

O2 + 2H+

H2O

Acetaldehyde

Ethanol

TCA Cycle

Stresses on plant Stresses on plant Decrease in Cell Energy Charge

Can’t produce or maintain enzymes and cell membrane Glycosidic acidosis due to loss of ion gradientsGlycosidic acidosis due to loss of ion gradientsHormonal imbalance

Accumulation of toxic compounds under anaerobic metabolism (acetaldehyde, ethanol)Cyanogenesis

Hydrolysis of cyanogenic glycosides produce CyanideDeath by Anaerobic Starvation

Inefficient metabolism of non structural carbohydrates

Water BalanceSuberization and loss of root area for water uptake

5

Adaptation to soil anaerobiosisAdaptation to soil anaerobiosisAdaptation to soil anaerobiosisAdaptation to soil anaerobiosisPhysiological Adaptations

Anaerobic respirationAnaerobic respirationAlternative metabolic byproducts

Morphological AdaptationsExternal: Prop roots, Pneumatophores, Lenticels, Stem Elongation,Internal: Aerenchyma, Hypertrophied Stems

Oxidized RhizosphereOxidizing the root environment via radial oxygen lossPrecipitation of dissolved metals in the root zoneOxidation of reduced compounds in the root zone

How Does Oxygen/Air How Does Oxygen/Air ygygEnter the Plant?Enter the Plant?

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Stomates

Typically associated Typically associated with leaves, can be found on herbaceous stems.Open and closed by guard cells, regulated by CO2 and moisture.Li k b tLink between atmosphere and vascular bundles.

http://www.cropsci.uiuc.edu/ocgs/cpsc399/PlantsystemsSu02.htm

LenticelsPores that form between the atmosphere and the cambium l f t d t klayer of stems and trunksTriggered by ethylene productionOnly occur on woody speciesIncrease gas transfer to the cambiumHave greatest concentration near the air water interfaceHave been shown to influence O2 concentration in Red Mangrove prop roots by 90% if blocked.

7

XylemOuter Bark

Lenticels

O2

O2

O2

O2

Lenticels

PhloemCortex

CO2CH4

O2O2

Prop RootsProp RootsModified root, only found in Red Mangrove Speciesin Red Mangrove SpeciesEach Root originates from the trunk above the water surfaceRoots are very spongy and porousLenticels on roots just above the air/water interface provide connection with atmospheric oxygenOxygen concentration measured in roots as high as 15-18%

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PneumatophoresModified root

perpendicular to main t i h i t lroots running horizontal

just below the sediment surfaceFound only in Black Mangrove speciesLenticels on root provideLenticels on root provide connection to atmospheric O2 when exposed above the water surface

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Mangrove

AirCO2

Water

Pneumatophores

Soil

Stem / PetioleStem / PetioleElongationElongation

Elongation of stem not i t d ith llassociated with cell

replication.Triggered by inundation and most likely linked to increases in ethylene concentration.Maintains connectionMaintains connection between atmospheric oxygen and below-water organs of the plant.

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What are the Internal What are the Internal Passageways for Gas Transfer?Passageways for Gas Transfer?

Hypertrophied Hypertrophied StemStem

Swelling along stem/trunk not associated with growth but resulting from the enlargement of cellsButtressing in treesExpanded tissue canExpanded tissue can provide passageway for gases between the atmosphere and below-water tissue

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AerenchymaAerenchyma

Genetically predisposedDevelop with growthSensitive to ethylene induced cellulase

InducedResponse to increased concentration of ethyleneethylene

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AerenchymaAerenchymaGenetically PredisposedGenetically Predisposed

Cattail RootT hTypha latifolia

Aerenchyma (intercellular air space)

Induced AerenchymaInduced Aerenchyma

Synthesis of 1-aminocyclopropand-1-carboxylic acid

(ACC)

Primary Root

(ACC)

10 cm

O2 Ethylene ACCACC

aerobic 2 day anaerobic 4 day anaerobic

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Porosity influenced by redox potentialPorosity influenced by redox potential

30

40

sity

(%) a

bb

10

oss

oo

t d-1

)20

10

0

Roo

t por

os

bb

5

0

-200200 -300

Eh (mV)

Rad

ial O

2lo

(μm

ol g

-1dr

y ro

a

Kludze and DeLaune, Sci. Soc. Am J., 1938)

How do Gases Move InsideHow do Gases Move InsideHow do Gases Move Inside the Plant?

How do Gases Move Inside the Plant?

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Oxygen movementOxygen movementthrough the plant through the plant

DiffusionDiffusion - due to partial pressure diffdifferencesConvective / Mass flowConvective / Mass flow - due to total pressure differences as a result of thermo-osmotic pressure differences at the leaf surface.

Temperature inducedpHumidity inducedCO2 solubilizationVenutri effect

1 meter

15

1 meter

Atmosphere

Rhi

Water

Old LeafNew Leaf

Rhizome

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Upper Leaf Surface

Leaf SectionLeaf Section

Porous Partition (<0.1 mm)

StomataN2

Surface

Lower Leaf Surface

EnergyInternal PressurizationInternal PressurizationTemperature Induced Temperature Induced

T0 P0

PorousPartition

(< 0.1 um)

T1T2P1

P2

T1 = T2 > T0

P1 > P2 > P0

PorousPartition

(> 0.1 um)

old leafnew

leaf

T0 = temperature outsideT1 = temperature inside new leafT2 = temperature inside old leaf

P0 Pressure outsideP1 Pressure inside new leafP2 Pressure inside old leaf

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Effect of temperature and age of leafEffect of temperature and age of leaf

120

100

ΔT = 1K

ΔT = 5K100

80

60

40

(mL

air h

-1)

ΔT = 8K

20

0Young Old

Leaf AgeGrosse, 1989

Internal PressurizationHumidity Induced

Internal PressurizationHumidity Induced

[ H2O ]o[O2 , CO2 , N2]0

P

Energy

PorousPartition

(< 0.1 um)

PorousPartition

(> 0.1 um)

old leafnew

leaf

[ H2O ]1[ H2O ]2[ O2 ]1

[ O2 ]2

[H2O]1 = [H20]2 > [H20]o

[O2, CO2, N2]1 > [O2, CO2, N2]o

P0

P1P2

[H2O]0 = Humidity outside[H2O]1 = Humidity inside new leaf[H2O]2 = Humidity inside old leaf

[O2]0 Concentration outside[O2]1 Concentration inside new leaf[O2]2 Concentration inside old leaf

P0 Pressure outsideP1 Pressure inside new leafP2 Pressure inside old leaf

P1 > P2 > P0

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AtmosphereAir Intake

Young Leaves

Old Leaves

Air IntakeAir Exhaust

Water

Floodwater

Air Intake

Air Exhaust

RhizomeSoil

Rhizome

Mass flow –CO2 Solublization

Mass flow –CO2 Solublization

Water

Air Air

Plant

CO2

CO2

Air

N2

CO2

O

O2

Air

O2

O2

CO2(aq)

HCO⇆CO 2

O2

O2

O2

N2

N2

Leaf Water

N2CO2

O2

CO2

O2

O2

CO2(aq)

HCO3-⇆CO3

2-

O2

(Redrawn from Taskin, I., and Kende, H., Science 1985)

O2

N2

19

peed

Mass flow - Venturi Effect

Air

Win

d sp

Air

Drained SoilDrained Soil

Gas Exchange in Soil / Water / Plant System

Flooded SoilFlooded Soil

OO22

OO22

COCO22CO2, CH4, andother gases

Dissloved metalssulfides, and organic acids

?

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Oxidized RhizosphereOxidized RhizosphereMost adaptations discussed relate to longitudinal transfer of oxygen to root.Oxygen concentration inside root is high, oxygen concentration outside root low/absentStrong concentration gradient can results in radial oxygen loss (ROL) forming an Oxidized Rhizosphere.

Oxygen Levels in Root and Oxidized Rhizosphere (cross section)

Phragmities australis7mm back from apex

W. Armstrong et al 2000, Annals of Botany 86:687-703

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Oxygen Levels in Root and Oxidized Rhizosphere (cross section)

Phragmities australis100 mm back from apex

W. Armstrong et al 2000, Annals of Botany 86:687-703

Oxygen Levels in Root and Oxidized Rhizosphere (longitudinal profile)

T. D. Colmer, 2003, Plant, Cell and Environment 26, 17-36

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Conceptual model of oxidized rhizosphere with barrier to ROL near

root base

Oxygen Flux Phargmites australis

O2 Flux

2.08 g/m2 dayg y

Root Respiration2.06 g/m2 dayNet Release

0.02 g/m2 dayBrix and Schierup, 1990

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CarbonCarbon NitrogenNitrogen

Oxidation-Reduction

O2 + Aerobic soil

Anaerobic soil

O2

NO3- NH4

+O2 + Aerobic soil

Anaerobic soil

O2

OMCO2

OM NH4+OM VFA

IronIron ManganeseManganese

Oxidation-Reduction

O2 + Aerobic soil

Anaerobic soil

O2

Mn4+ Mn2+O2 + Aerobic soil

Anaerobic soil

O2

Fe2+Fe3+

Mn4+ Mn2+Fe3+ Fe2+

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Oxidizing Activity of Roots

Toxicity of reduced compounds (e.g., lfid ) i d dsulfides) is decreased.

Supports nitrification and methane oxidation.Precipitates metals and in some cases nutrient uptake is decreasednutrient uptake is decreased.

Does Gas Transport Only Occur Does Gas Transport Only Occur p yin One Direction?

p yin One Direction?

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O

Methane Exchange Through Plant

CH4

CO2

O2

WaterO2 + CH4 CO2

Atmosphere

SoilCH4

2 4 CO2

CH4 O2 CO2+

100

80 Methaneur

Gas Exchange through PlantsGas Exchange through Plants

60

40

20

Methane

Oxygen

flux,

mg/

m2

hou

Sagittaria Canna Scirpus Scirpus Typha Pontederia

0

latifolia flaccida pungens validus latifolia cordata

Emergent aquatic macrophytes

Gas

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Learning Objectives Summary

Loss of oxygen has significant implications for plant metabolism/survival.

W tl d d t d l t h h i l i l dWetland adapted plants have numerous physiological and morphological adaptations to deal with these stresses.

Movement of gases within the plant is the result of a combination of diffusive and convective mechanisms.

Radial oxygen loss from roots result in an oxidized rhizosphere that significantly increases the aerobicrhizosphere that significantly increases the aerobic-anaerobic interface in a wetland and can reduce anaerobic stress on vegetation.

Gas exchange is bidirectional: oxygen in - reduced gases out.