Effects of Genotype and Environment on the Plant Ionome

Home , Berberidopsidales, Brassicales, Caryophyllales, Crossosomatales, Dipsacales, Fabales

Philip J. White Martin R. Broadley

and many others

FertBio2014 18th September 2014 Ionomics is the Study of the Elemental Composition of Plants

98.5 % Carbon (Sodium)

Oxygen Chlorine Hydrogen Boron

Nitrogen Iron Potassium Manganese Calcium Zinc Magnesium Copper (Silicon) Nickel Phosphorus Molybdenum Sulphur (Cobalt, Iodine, Vanadium, Selenium)

...and every other element in the periodic table available in the environment Phylogenetics Genetics at a Higher Level of Classification

Phylogenetics is the study of the relationships among groups of organisms (e.g. families, species, populations) based on DNA sequencing.

The result of phylogenetic studies are hypotheses about the evolutionary history of taxonomic groups.

Angiosperms – flowering plants.

A definition of phylogenetics and its utility Phylogenetics Angiosperm Phylogeny

The Angiosperm Phylogeny Group (1998, 2003, 2009) Fagales Cucurbitales Rosales Fabales Oxalidales Malpighiales Celastrales Angiosperms Zygophyllales Myrtales Sapindales (flowering plants) Malvales Brassicales Crossosomatales Geraniales 250,000 species Vitaceae Saxifragales Berberidopsidales 462 families Dipsacales Apiales eudicots Asterales 47 orders Aquifoliales Lamiales Solanales Gentianales Garryales Cornales APG II (2003) Ericales Caryophyllales Dilleniaceae Santanales Gunnerales Trochodendraceae Buxaceae/Didymeleaceae Sabiaceae Proteales Ranunculales Ceratophyllales Winterales Magnoliales Laurales Piperales monocots basal angiosperms Chloranthales Illiciaceae and magnoliids Schisandraceae Austrobaileyaceae Nymphaceae Amborellaceae monocots - commelinoids

Grass Bromeliad

Costus

Bamboo Banana monocots - non-commelinoid Caryophyllales asterids rosids Plant Species Differ in Their Ionome

Functional Foods

Fertiliser Use Efficiency

Tolerant Crops Safer Crops Phytoremediation Contaminant Transfer Evolution of the Angiosperm Ionome Selected Examples

(1) Calcium, Strontium & Magnesium

(2) Silicon

(3) Sodium (in nonsaline environments)

(4) Rothamsted Park Grass Experiment

FertBio2014, Araxá, Brazil, 18th September 2014 Evolution of the Angiosperm Ionome Data Sources

MetaMeta-analysis-Analyses of literature of data Comparative(182 comparative Studies studies in 40 papers)

Experiments under Controlled Conditions Botanical Surveys

Insights to the Angiosperm Ionome – Sources of Data A Botanical Journey Through The Periodic Table

Group II Elements

Broadley et al. (2003) J. Exp. Bot. 54, 1431-1446 Broadley et al. (2004) J. Exp. Bot. 55, 321-336 Magnesium : Calcium Ratios in Shoot Tissues

Hydroponics Sampled from the field 2.0 2.0

1.5 1.5

(%)

(%) 1.0 1.0

shoot

[Mg]

[Mg] 0.5 0.5

0.0 0.0 0 1 2 3 4 5 0 1 2 3 4 5

[Ca]shoot (%) [Ca]shoot (%) Magnesium : Calcium Ratios in Shoot Tissues

Hydroponics Sampled from the field 2.0 2.0

1.5 1.5

(%)

(%) 1.0 1.0

shoot

[Mg]

[Mg] 0.5 0.5

0.0 0.0 0 1 2 3 4 5 0 1 2 3 4 5

[Ca]shoot (%) [Ca]shoot (%)

 All other taxa  Caryophyllales (e.g. sugar beet, carnation) Fagales Cucurbitales Rosales Shoot Mg / Ca Ratios Fabales Oxalidales (n=1) Malpighiales of Angiosperm Orders Celastrales Zygophyllales Myrtales Sapindales Malvales > 200 species Brassicales Crossosomatales Geraniales grown hydroponically Vitaceae Saxifragales Berberidopsidales Dipsacales Apiales Asterales Aquifoliales high 0.8 Lamiales Solanales Gentianales Garryales mean Cornales Ericales Caryophyllales (n=51) Dilleniaceae low 0 Santanales Gunnerales Trochodendraceae Buxaceae/Didymeleaceae Sabiaceae Proteales Ranunculales Ceratophyllales Winterales Magnoliales Laurales Piperales monocots Chloranthales Illiciaceae Schisandraceae Austrobaileyaceae Nymphaceae Amborellaceae Shoot Mg / Ca Ratios in the Caryophyllales

51 species Plumbaginaceae Polygonaceae grown hydroponically

Caryophyllaceae Amaranthaceae

Aizoaceae

Phytolaccaceae

Nyctaginaceae high 1.2

Cactaceae Portulacaceae mean low 0 Ecological Implications - Serpentine Flora

name is derived from the mineral serpentine

((Mg,Fe)3Si2O5(OH)4)

high Mg and Fe; low Ca high Ni, Cr and Co; low organic matter; little water; low N, P and K

Edmonstons Chickweed - Cerastium nigrescens (Caryophyllaceae). World distribution restricted to the serpentine debris on Unst

Proctor J (1999) Toxins, nutrient shortages and droughts: the serpentine challenge. Trends in Ecology and Evolution, 14, 334-335 Magnesium : Calcium Ratios in Shoot Tissues

Hydroponics Sampled from the field 2.0 2.0

1.5 1.5

(%)

(%) 1.0 1.0

shoot

[Mg]

[Mg] 0.5 0.5

0.0 0.0 0 1 2 3 4 5 0 1 2 3 4 5

[Ca]shoot (%) [Ca]shoot (%)

 All other taxa  Caryophyllales (e.g. sugar beet, carnation) Magnesium : Calcium Ratios in Shoot Tissues

Hydroponics Sampled from the field 2.0 2.0

1.5 1.5

(%)

(%) 1.0 1.0

shoot

[Mg]

[Mg] 0.5 0.5

0.0 0.0 0 1 2 3 4 5 0 1 2 3 4 5

[Ca]shoot (%) [Ca]shoot (%)

 All other taxa  Caryophyllales (e.g. sugar beet, carnation)  Poales (e.g. the grass / cereal family, Poaceae) Magnesium : Calcium Ratios in Shoot Tissues

Hydroponics Sampled from the field 2.0 2.0

1.5 1.5

(%)

(%) 1.0 1.0

shoot

[Mg]

[Mg] 0.5 0.5

0.0 0.0 0 1 2 3 4 5 0 1 2 3 4 5

[Ca]shoot (%) [Ca]shoot (%)

 All other taxa  Caryophyllales (e.g. sugar beet, carnation)  Poales (e.g. the grass / cereal family, Poaceae)  Asterales (e.g. the daisy / sunflower family Asteraceae) Fagales Cucurbitales Rosales Shoot Ca Concentrations Fabales Oxalidales Malpighiales of Angiosperm Orders Celastrales Zygophyllales Myrtales Sapindales Malvales Brassicales

Geraniales

Eudicots > monocots Saxifragales

Dipsacales Apiales Asterales

Lamiales high 3 % Solanales Gentianales

Ericales Caryophyllales

low 0

Proteales Ranunculales

Magnoliales Laurales Piperales monocots Chloranthales Illiciaceae Schisandraceae Austrobaileyaceae Nymphaceae Amborellaceae Shoot Calcium Concentrations of Monocot Orders

Zingiberales high 1.5% Commelinales Poales commelinoid monocots low 0 Arecales Asparagales

non- commelinoid monocots Dioscoreales Alismatales

shoot Ca concentrations of different monocot orders differ non-commelinoid monocots > commelinoid monocots (Poales, Arecales) Plant Calcium - Dietary Consequences

calcium deficiency disorders arise when populations change from bean-rich to cereal-rich diets

Thacher (2006) Ann. Trop. Paediatrics 26, 1-16 White & Broadley (2009) New Phytol. 182, 49-84 Strontium : Calcium Ratios In Shoots of 44 Plant Species

100 90 80 70 60 50 40

30 Poales 20 10

Strontium content Strontium(µCi/g) content 0 0 10 20 30 40 Calcium content (mg/g)

Andersen AJ (1967) Risö Report 170 Phylogenetic Variation in

Shoot Mineral Concentrations

Proportion of genetic variation Ca Mg Sr order and above (%) 64 65 76

within order (%) 36 35 24

Ancient evolutionary origin of variation in Ca, Mg & Sr concentrations

Broadley et al. (2004) J. Exp. Bot. 55, 321-336 A Botanical Journey Through The Periodic Table

Silicon

Hodson et al. (2005) Ann. Bot. 96, 1027-1046 Silicon in Plants

6060 Non-commelinoid monocots (onion) 50 Asterids (daisy) 4040

2020

% frequency of observations all frequency % 00 00 22 44 66 88 1010 1212 1414 % Si in leaf tissue

Hodson et al. (2005) Ann. Bot. 96, 1027-1046 Silicon in Plants

70 Commelinoid monocots (grass) 6060 Non-commelinoid monocots (onion) 50 Asterids (daisy) 4040

2020

% frequency of observations all frequency % 0 0 2 4 6 8 10 12 14 0 2 4 6 8 10 12 14 % Si in leaf tissue

Hodson et al. (2005) Ann. Bot. 96, 1027-1046 Silicon in Plants

Proportion of genetic variation Ca Mg Sr Si order and above (%) 64 65 76 80

within order (%) 36 35 24 20

Ancient evolutionary origin of variation in Ca, Mg, Sr & Si concentrations

Ca, Mg, Sr : eudicots ≥ non-commelinoid monocots > commelinoid monocots Si : eudicots ≤ non-commelinoid monocots < commelinoid monocots Variation in Ionomes of Angiosperm Species

I II III IV V VI VII VIII

H He Li Be B C N O F Ne ancient Na Mg Al Si P S Cl Ar K Ca Ga Ge As Se Br Kr Rb Sr In Sn Sb Te I Xe Cs Ba Tl Pb Bi Po At Rn recent

Watanabe et al. (2007) New Phytol. 174, 516-523 Distribution of Leaf Sodium Concentrations Among Angiosperm Species

Evolution of Sodium Accumulation in the Caryophyllales Distribution of Leaf Sodium Concentrations Among Angiosperm Species

Evolution of Sodium Accumulation in the Caryophyllales Fagales Cucurbitales Rosales Shoot Sodium Concentrations Fabales Oxalidales Malpighiales of Angiosperm Orders Celastrales Zygophyllales Myrtales Sapindales Malvales 311 species Brassicales Crossosomatales Geraniales grown hydroponically Vitaceae Saxifragales Berberidopsidales Dipsacales Apiales Asterales Aquifoliales high 0.5 Lamiales Solanales Gentianales Garryales Cornales mean Ericales low Caryophyllales (n=63) 0 Dilleniaceae Santanales Gunnerales Trochodendraceae Buxaceae/Didymeleaceae Sabiaceae Proteales Ranunculales Ceratophyllales Winterales Magnoliales Laurales Piperales Monocots (8 orders) Chloranthales Illiciaceae Schisandraceae Austrobaileyaceae Nymphaceae Amborellaceae Phylogenetic Effects on the Plant Ionome

<0.1 0.1-0.5 0.5-1.0 1.0-1.5 1.5-2.0 >2.0

Evolution of Sodium Accumulation in the Caryophyllales Phylogenetic and Environmental Effects on the Plant Ionome

Park Grass, Rothamsted 1856-2014 Botanical Composition of Park Grass Plots (Crawley et al., 1991-2000)

Crawley et al. (2005) American Naturalist 165, 179-192 Phylogenetic and Environmental Effects on the Plant Ionome

White et al. (2012) New Phytologist 196, 101-109 Plant Species Differ in Their Ionome

4 Polygonaceae Fabaceae 2 Apiaceae

0 Ranunculaceae Asteraceae -2 Poaceae

-4

Discriminant Score 2 Score Discriminant Plantaginaceae -6

-8 -6 -4 -2 0 2 4 6 8 Discriminant Score 1

White et al. (2012) New Phytologist 196, 101-109 Calcium : Magnesium Ratios

DW) 8

-1 6 Polygonaceae (Caryophyllales) 4 other Angiosperm families 2

Shoot Mg (mg g (mg Mg Shoot 0 Poaceae 0 10 20 30 40 Shoot Ca (mg g-1 DW)

White et al. (2012) New Phytologist 196, 101-109 Phylogenetic and Environmental Effects on the Plant Ionome

White et al. (2012) New Phytologist 196, 101-109 Evolution of the Angiosperm Ionome

Plant Species Differ in their Ionome

Differences Attributed to Ancient and Recent Evolutionary Events

Commelinoid monocots - low Calcium, Magnesium, Strontium Commelinoid monocots - high Silicon Caryophyllales - high Magnesium / Calcium Ratios Some Caryophyllales (hyper)accumulate Sodium

(Phylo)genetic Variation exceeds Environmental Variation For some Elements

FertBio2014, Araxá, Brazil, 18th September 2014 Evolution of the Angiosperm Ionome

Plant Species Differ in their Ionome

Differences Attributed to Ancient and Recent Evolutionary Events

Commelinoid monocots - low Calcium, Magnesium, Strontium Commelinoid monocots - high Silicon Caryophyllales - high Magnesium / Calcium Ratios Some Caryophyllales (hyper)accumulate Sodium

(Phylo)genetic Variation exceeds Environmental Variation For some Elements

FertBio2014, Araxá, Brazil, 18th September 2014