image
image
image
image
image
image
image
image
 
Pflanzliche Anpassung an
Phosphor
verfügbarkeit
illnitz
9. November 2016

image
image
image
image
image
image
image
 
Stress- und Entwicklungsbiologie
(Scheel)
Stoffwechsel- und Zellbiologie
(Tissier)
Molekulare Signalverarbeitung
(Abel)
Natur- und Wirkstoffchemie
(Wessjohann)
Leibniz-Institute für Pflanzenbiochemie, Halle

image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
 
CO
2
H
2
O
K
P
B
Cl
Mn
Fe
Zn
Cu
Mo
Ni
Se
Na
S
Mg
Ca
Essential Plant Mineral Nutrients
N
2
N

image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
 
B
Cl
Mn
Fe
Zn
Cu
Mo
Ni
Se
Na
S
Mg
Ca
“Why nature chose phosphate?”
Westheimer (1987) Science 235:1173-1178
CO
2
H
2
O
K
P*
N
2
N

image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
 
-
H
2
O
CO
2
NO
3
-
SO
4
2-
HPO
4
2-
Light
CHO
-NH
2
-SH
NADPH
“Why nature chose phosphate?”
Westheimer (1987) Science 235:1173-1178
HPO
4
2-

image
image
image
image
image
image
image
image
image
image
image
image
image
image
 
“Bioenergetics” of Macronutrient Assimilation
Electronegativity
Energy Requirements for Reduction
3.4
Polarity
(X O)
Reduction
(X● ●O)
O
O
NAD(P)H
NH
3
NO
-
3
3.0
N
O
NAD(P)H + ATP
CO
2
SO
2-
4
H
2
S
CHO
NAD(P)H + ATP
2.6
2.6
S
O
C
O
Solar Energy
H
2
O
{H
2
}
PO
3
4
-
PH
3
?
2.2
2.1
O
O
H
P

image
image
image
image
image
image
image
image
image
 
HPO
4
2-
CHO
-P
Photosynthetic Reactions
HPO
4
2-
Phosphorus and Hesperus
Evelyn De Morgan (1889)
Phōsphoros:
“The bearer of light”
“Light”
“Dark”
ADP
~
P

image
image
image
image
image
image
image
image
 
O
||
|
O
-
O
|
|
O
|
|
R
1
R
2
Membranes
Hydrolysis (OH
-
)
P
HPO
4
2-
CHO
-P
Photosynthetic Reactions
HPO
4
2-
Charged Diesters
(e.g., nucleic acids)
ATP
“Light”
“Dark”

image
image
image
image
image
image
image
image
image
image
 
HPO
4
2-
CHO
-P
Photosynthetic Reactions
HPO
4
2-
ATP
“Light”
“Dark”
IP
6
: Auxin Receptor
IP
5
: Jasmonate Receptor
P
P
P
Proteins
P
_
P
_
P~
~P
Inositol Polyphosphates (IP
3
– IP
8
)
P
P
P

image
image
image
image
image
image
image
image
image
image
image
 
HPO
4
2-
ATP
“Light”
“Dark”
CHO
-P
Photosynthetic Reactions
Ca
2+
Chemical Rationale for Calcium Signaling
O
||
|
O
-
|
|
O
|
H
P
O
-
Me
>2+
O
46.6
Si
27.7
Al
8.1
Fe
5.0
Ca
3.6
Na
2.8
K
2.6
Mg
2.1
Elemental
Abundance
(%)
Lithosphere
K
sp
of
Phosphates
(10
-20
...10
-44
)
P
0.1

image
image
image
image
image
image
image
image
image
image
 
HPO
4
2-
ATP
“Light”
“Dark”
CHO
-P
Photosynthetic Reactions
Ca
2+
Chemical Rationale for Calcium Signaling
O
||
|
O
-
|
|
O
|
H
P
O
-
Al
3+
Aluminium Toxicity
O
46.6
Si
27.7
Al
8.1
Fe
5.0
Ca
3.6
Na
2.8
K
2.6
Mg
2.1
Elemental
Abundance
(%)
Lithosphere
K
sp
of
Phosphates
(10
-20
...10
-44
)
P
0.1

image
image
image
image
image
image
image
image
image
image
image
image
 
HPO
4
2-
ATP
“Light”
“Dark”
CHO
-P
Photosynthetic Reactions
Ca
2+
Chemical Rationale for Calcium Signaling
O
||
|
O
-
|
|
O
|
H
P
O
-
Al
3+
< 2
µ
M
> 1 mM
Organic-P
(30-95%)
Insoluble
P-Salts
Rhizosphere
HPO
4
2-
Low P
Bioavailability
Aluminium Toxicity

image
 
Limited
P Bioavailability
on a Global Scale
4
5
6
7
8
9
10
P
Ca, Mg
Fe
Al
Insoluble Fe- and Al-
phosphates
Insoluble Ca- and Mg-
phosphates
Acidic (low P)
Neutral
Basic (low P)
World Soils
(Source: FAO)
pH

image
image
image
image
 
https://www.agric.wa.gov.au/mycrop/
phosphorus-deficiency-wheat
No P-Fertilization
Australia
P-Fertilization

image
image
image
image
 
Hypericum hidcote
(Großblumiges Johanniskraut)
No P-Fertilization
P-Fertilization
http://www.manna.de

image
image
 
Nature, October 2009

image
image
 
Scientific American, June 2009

image
image
image
image
image
 
Annual use of P-fertilizers worldwide: > 40 Million tons (ca. $25 Billion)
Phosphorite or rock phosphate (15-25% P)
Typical sedimentary rock (<0.2% P)

image
image
image
image
image
 
Heavy Metal Contamination and Eutrophication

image
image
image
image
image

image
image
image
image
image
image
image
image
image
 
N
2
Pi
Fe
Al
Mg
Ca
N
K
Plant Responses to
Phosphate (Pi)
Limitation

image
image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Reduced photosynthesis
Reduced shoot growth
+Pi
–Pi

image
image
image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Reduced photosynthesis
Reduced shoot growth
Anthocyanin synthesis

image
image
image
image
image
image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Anthocyanin synthesis
Starch and sugar synthesis
Transitory Starch
Reduced photosynthesis
Reduced shoot growth

image
image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Transitory Starch
ADP +
Pi
AT
P
AT
P
+ CO
2
Triose-
P
+ ADP
nTriose-
P
Hexoses/Starch +
Pi
Chloroplast

image
image
image
image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Anthocyanin synthesis
Starch and sugar synthesis
Lipid remodeling
High Pi
Low Pi
P-Lipids
P-free
Lipids
Carini et al. (2015) PNAS 112:7767-7772
Reduced photosynthesis
Reduced shoot growth

image
image
image
image
image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Anthocyanin synthesis
Starch and sugar synthesis
Pi recycling and remobilization
Pi
Reduced photosynthesis
Reduced shoot growth
Lipid remodeling

image
image
image
image
image
image
image
image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Anthocyanin synthesis
Starch and sugar synthesis
Pi high affinity uptake
Exudation (Pi mobilization)
Pi
Organic acids
P-hydrolases
Reduced photosynthesis
Reduced shoot growth
Pi recycling and remobilization
Lipid remodeling

image
image
image
image
image
image
image
image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Anthocyanin synthesis
Starch and sugar synthesis
Pi high affinity uptake
Exudation (Pi mobilization)
Root system architecture
Reduced photosynthesis
Reduced shoot growth
Pi recycling and remobilization
Lipid remodeling

image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Anthocyanin synthesis
Starch and sugar synthesis
Root system architecture
Mycorrhiza formation
Pi high affinity uptake
Exudation (Pi mobilization)
Carbohydrates
(e.g., Sucrose)
Mineral Nutrients
(e.g., Phosphate)
Reduced photosynthesis
Reduced shoot growth
Pi recycling and remobilization
Lipid remodeling

image
image
image
image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Local Responses: External Pi Supply
Pi
Pi Acquisition
Systemic Responses: Internal Pi Status
Pi
Pi Recycling

image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Systemic Responses: Internal Pi Status
Nucleic Acids
Lipid P
Ester P
Free Pi
Total Leaf Phosphorus: 0.1 - 0.3% of DW
Veneklaas et al. (2012) New Phytol 195:306-320

image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Systemic Responses: Internal Pi Status
Free Pi
Cytoplasm
5 mM
145 mM
26 mM
35 mM
Vacuoles
Low Pi
High Pi
Mimura et al. (1990) Planta 180:139-146
~
<<

image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Systemic Responses: Internal Pi Status
Systemic
miR399
PHR1
Target Genes
PHR1
SPX1
Pi
Nucleus
Pi
Pi
Pi
Vacuole
Pi
Transcription factor
Repressor

image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Systemic Responses: Internal Pi Status
Systemic
miR399
Nucleus
Pi
Vacuole
PHR1
Metabolic Adjustments
PHR1
Target Genes
SPX1
Pi
Pi
Pi
PHR1
SPX1
Pi
Transcription factor
Repressor

image
image
image
image
image
image
image
image
image
 
Plant Responses to
Phosphate (Pi)
Limitation
Local Responses: External Pi Supply
Pi
Pi Acquisition
Systemic Responses: Internal Pi Status
Pi
Pi Recycling

image
image
image
image
image
image
image
image
image
 
N
2
Pi
Fe
Al
Mg
Ca
N
K
Plant Responses to
Phosphate (Pi)
Limitation

image
image
image
image
image
image
image
 
Pedogenesis
>2,000,000 yrs
Parent rock (igneous/metamorphic)
>1,000
ppm
Rock weathering
Ca
5
(PO
4
)
3
(F,OH,Cl)
Leaching
Rock
Basic Soils
Acidic Soils
Walker and Syers (1976) Geoderma
Fe, Al oxides/hydroxides
<<100
Geochemistry and Ecology
Fate of Phosphorus during Soil Development

image
image
image
 
Richardson et al. (2004) Oecologia
Example
: Franz Josef Gacier Soil Chronosequence
Western Australia

image
 
Turner and Laliberté (2015) Ecosystems
Example
: The Jurien Bay Soil Chronosequence
Western Australia

image
image
image
image
 
Example
: The Jurien Bay Soil Chronosequence
pH

image
 
Limited
P Bioavailability
on a Global Scale
4
5
6
7
8
9
10
P
Ca, Mg
Fe
Al
Insoluble Fe- and Al-
phosphates
Insoluble Ca- and Mg-
phosphates
Acidic (low P)
Neutral
Basic (low P)
World Soils
(Source: FAO)
pH

image
 
Pi-diffusion rate
<<
Pi-uptake rate
Root system expansion for
Pi interception
Competition with microorganisms
Different Phosphate (Pi) Acquisition Strategies

image
image
image
image
image
 
Mycorrhiza
Topsoil Foraging
P Scavenging
Brassicaceae-type
Different Phosphate (Pi) Acquisition Strategies
Cluster Roots
P Mining
Proteaceae-type
Org.
Acids
+
-
Pi
Fe
7-20%
Carbon Cost
25-50%

image
image
image
image
 
Mycorrhiza
Topsoil Foraging
P Scavenging
Brassicaceae-type
Different Phosphate (Pi) Acquisition Strategies
Cluster Roots
P Mining
Proteaceae-type
Org.
Acids
+
-
Pi
Fe
Responses to
Pi Deficiency (Most Soils)
Adaptation to
Pi Impoverished Soils

image
 
Adaptation of Proteaceae-type Species
Lambers et al. (2015) Nat Plants
1 cm
1-5
6-10
11-15
16-20
d
Cluster Roots (
exudative burst
)
Organic acids (anion exchange)
Phospho-hydrolases
Phenolics (antimicrobial)
Cell wall-degrading enzymes
High P remobilization (senescence)
Remodeling of membrane lipids
Altered rRNA profiles
Delayed greening
Preferential P allocation to mesophyll
High seed P content
Shoot Pi Economy

image
image
image
 
Parent rock (igneous/metamorphic)
>1,000
ppm
Rock weathering
Ca
5
(PO
4
)
3
(F,OH,Cl)
Leaching
Fe, Al oxides/hydroxides
<<100
Geochemistry and Ecology
non-mycorrhizal
Proteaceae-type
P Mining
Different Phosphate (Pi) Acquisition Strategies

image
image
image
image
image
image
image
image
image
image
image
 
Fe(II)
Fe(III)
oxides
Silicates, Sulfides
Rock weathering (O
2
exposure)
Very small (5–150 nm) and poorly ordered crystals
Extremely
low
solubility
K
sp
~10
-40
Goethite
Hypoxic Conditions
Iron
oxyhydroxide
(
α
-FeOOH)
Strong
Very large specific surface area (50-300 m
2
g
-1
)
Pigments
Fe oxides: <0.1% to >50% of total soil mass

image
image
image
image
image
image
image
image
 
Fe(III)
oxides
Adsorption of HPO
4
2-
to Fe oxides
Lambers et al. (2015) TIPS
(Up to 2.5
µ
mol P m
-2
or 0.75 mmol P g
-1
)
Competitive
desorption by „natural organic matter“
(
citric, malic, humic, fulvic acids
),
pH dependent
Ca
2+
promotes HPO
4
2-
adsorption
Only 30-60% of adsorbed HPO
4
2-
is exchangeable,
low mobility

image
image
image
image
image
image
image
image
image
 
Fe(III)
oxides
Adsorption of HPO
4
2-
to Fe oxides
Lambers et al. (2015) TIPS
(Up to 2.5
µ
mol P m
-2
or 0.75 mmol P g
-1
)
Competitive
desorption by „natural organic matter“
(
citric, malic, humic, fulvic acids
),
pH dependent

image
image
image
 
Parent rock (igneous/metamorphic)
>1,000
ppm
Rock weathering
Ca
5
(PO
4
)
3
(F,OH,Cl)
Leaching
Fe, Al oxides/hydroxides
<<100
Geochemistry and Ecology
2
µ
M Pi
mycorrhizal
0.5
µ
M Pi
P Scavenging
non-mycorrhizal
Proteaceae-type
P Mining
non-mycorrhizal
Brassicaceae-type
Different Phosphate (Pi) Acquisition Strategies

image
image
 
Arabidopsis thaliana
(Ackerschmalwand)
+Pi
–Pi

image
 
Arabidopsis thaliana
(Ackerschmalwand)

image
image
image
image
image
image
image
image
image
image
image
image
image
image
 
Meristem
Elongation
Differentiation
High Pi
High Pi
Low Pi
Adaptation of
A. thaliana
(Brassicaceae-type)
13 mm
< 20 h
Low Pi
~ 3 d
0.5 mm

image
image
image
image
image
image
image
 
High Pi
Low Pi
High N
Low N
Pi
+
-
Fe
K
sp
~10
-40
Insoluble
Soluble
Topsoil Foraging (Brassicaceae-type Species)
High Pi
Low Pi

image
image
image
 
High
Low
Meristem
G1
G2
S
M
G1
G2
S
M
SCN
Elongation
Hormone
Action
Pi Sensing
Systemic
Local
How is Pi sensed in root development ?
High Pi
Low Pi

image
image
image
image
image
 
High Pi
Low Pi
High
Low
Meristem
SCN
Elongation
Role of Exudation
(organic acids
coumarines)
How is Pi sensed in root development ?
Pi
+
-
Fe
Pi
+
-
Al

image
image
image
image
image
image
 
Screen for
Pi deficiency response
Mutants
Pi
Pi-starvation
inducible Genes
Class I
Class II
Pi
Phospho-
hydrolases
Organic
-P
G1
G2
S
M
Root
-Pi
(+DNA)
-Pi
(+DNA)
+Pi (+DNA)
WT
pdr
WT
pdr

image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
image
 
Col
pdr2
pdr3
pdr4
pdr5
Forward Genetics
Ticconi et al. (2004) Plant J
Pi-deficiency response (pdr) Mutants
+Pi
–Pi
pCYCB1::GUS
Svistoonoff et al. (2007) Nat Genetics
Natural Variation (QTL)
LOW Pi ROOT (LPR1/LPR2)
+Pi
–Pi
pCYCB1::GUS

image
image
image
image
 
LPR1-PDR2: A Bridgehead in Pi Sensing
WT
pdr2
lpr1lpr2
lpr1lpr2
pdr2
pdr2
lpr1 lpr2
lpr1lpr2
WT
pdr2
High Pi
Low Pi
1 cm

image
image
image
image
image
 
QC25::GUS
Columella
(iodine staining
of amyloplasts)
Columella
Initials
Double-Staining of Quiescent Center
and Columella
Pi-dependent Inhibition of Root Meristem Activity
Meristem
Elongation
100
µ
m
Differentiation
+Pi
–Pi

image
image
image
image
image
image
image
image
image
image
 
Accelerated Loss of Stem Cell Identity in
pdr2
WT
+Pi (5 d)
+Pi (2 d)
–Pi (2 d)
Iodine
QC25
pdr2

image
image
image
image
image
image
image
image
image
image
image
image
image
image
 
PDR2
LPR1
Long Roots
Meristem Activity
Short Roots
High
P
Fe
Low
Callose
Deposition
Cell-to-Cell
Communication
SHR
SHR
16 h
ROS
SCN
SCN
Fe
,
Pi
Fe

image
image
image
image
image
image
image
 
Pflanzliche Anpassung an
Phosphor
verfügbarkeit
Prof. Steffen Abel
Leibniz-Institute für Pflanzenbiochemie, Halle (Saale)
Pillnitz, 9. November, 2016