Pflanzliche Anpassung an
Phosphor
verfügbarkeit
illnitz
9. November 2016
Stress- und Entwicklungsbiologie
(Scheel)
Stoffwechsel- und Zellbiologie
(Tissier)
Molekulare Signalverarbeitung
(Abel)
Natur- und Wirkstoffchemie
(Wessjohann)
Leibniz-Institute für Pflanzenbiochemie, Halle
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
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
-
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-
“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
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
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”
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
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
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
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
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
phosphorus-deficiency-wheat
No P-Fertilization
Australia
P-Fertilization
Hypericum hidcote
(Großblumiges Johanniskraut)
No P-Fertilization
P-Fertilization
Nature, October 2009
Scientific American, June 2009
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)
Heavy Metal Contamination and Eutrophication
N
2
Pi
Fe
Al
Mg
Ca
↓
N
K
Plant Responses to
Phosphate (Pi)
Limitation
Plant Responses to
Phosphate (Pi)
Limitation
•
Reduced photosynthesis
•
Reduced shoot growth
+Pi
–Pi
Plant Responses to
Phosphate (Pi)
Limitation
•
Reduced photosynthesis
•
Reduced shoot growth
•
Anthocyanin synthesis
Plant Responses to
Phosphate (Pi)
Limitation
•
Anthocyanin synthesis
•
Starch and sugar synthesis
Transitory Starch
•
Reduced photosynthesis
•
Reduced shoot growth
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
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
Plant Responses to
Phosphate (Pi)
Limitation
•
Anthocyanin synthesis
•
Starch and sugar synthesis
•
Pi recycling and remobilization
Pi
•
Reduced photosynthesis
•
Reduced shoot growth
•
Lipid remodeling
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
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
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
Plant Responses to
Phosphate (Pi)
Limitation
Local Responses: External Pi Supply
Pi
Pi Acquisition
Systemic Responses: Internal Pi Status
Pi
Pi Recycling
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
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
~
<<
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
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
Plant Responses to
Phosphate (Pi)
Limitation
Local Responses: External Pi Supply
Pi
Pi Acquisition
Systemic Responses: Internal Pi Status
Pi
Pi Recycling
N
2
Pi
Fe
Al
Mg
Ca
↓
N
K
Plant Responses to
Phosphate (Pi)
Limitation
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
Richardson et al. (2004) Oecologia
Example
: Franz Josef Gacier Soil Chronosequence
Western Australia
Turner and Laliberté (2015) Ecosystems
Example
: The Jurien Bay Soil Chronosequence
Western Australia
Example
: The Jurien Bay Soil Chronosequence
pH
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
Pi-diffusion rate
<<
Pi-uptake rate
Root system expansion for
Pi interception
Competition with microorganisms
Different Phosphate (Pi) Acquisition Strategies
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%
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
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
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
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
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
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
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
Arabidopsis thaliana
(Ackerschmalwand)
+Pi
–Pi
Arabidopsis thaliana
(Ackerschmalwand)
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
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
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
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
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
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
LPR1-PDR2: A Bridgehead in Pi Sensing
WT
pdr2
lpr1lpr2
lpr1lpr2
pdr2
pdr2
lpr1 lpr2
lpr1lpr2
WT
pdr2
High Pi
Low Pi
1 cm
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
Accelerated Loss of Stem Cell Identity in
pdr2
WT
+Pi (5 d)
+Pi (2 d)
–Pi (2 d)
Iodine
QC25
pdr2
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
Pflanzliche Anpassung an
Phosphor
verfügbarkeit
Prof. Steffen Abel
Leibniz-Institute für Pflanzenbiochemie, Halle (Saale)
Pillnitz, 9. November, 2016
