Effects of Genotype and Environment on the Plant Ionome

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1 Effects of Genotype and Environment on the Plant Ionome Philip J. White Martin R. Broadley and many others FertBio th September 2014

2 Ionomics is the Study of the Elemental Composition of Plants 98.5 % Carbon (Sodium) Oxygen Hydrogen Nitrogen Potassium Calcium Magnesium (Silicon) Phosphorus Chlorine Boron Iron Manganese Zinc Copper Nickel Molybdenum Sulphur (Cobalt, Iodine, Vanadium, Selenium)...and every other element in the periodic table available in the environment

3 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

4 Phylogenetics Angiosperm Phylogeny The Angiosperm Phylogeny Group (1998, 2003, 2009)

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

6 monocots - commelinoids Grass Bromeliad Costus Bamboo Banana

7 monocots - non-commelinoid

8 Caryophyllales

9 asterids

10 rosids

11 Plant Species Differ in Their Ionome Functional Foods Fertiliser Use Efficiency Tolerant Crops Phytoremediation Safer Crops Contaminant Transfer

12 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, 18 th September 2014

13 Evolution of the Angiosperm Ionome Data Sources Meta-analysis Meta-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

14 A Botanical Journey Through The Periodic Table Group II Elements Broadley et al. (2003) J. Exp. Bot. 54, Broadley et al. (2004) J. Exp. Bot. 55,

15 Magnesium : Calcium Ratios in Shoot Tissues Hydroponics Sampled from the field [Mg] shoot (%) 1.0 [Mg] shoot (%) [Ca] shoot (%) [Ca] shoot (%)

16 Magnesium : Calcium Ratios in Shoot Tissues Hydroponics Sampled from the field [Mg] shoot (%) 1.0 [Mg] shoot (%) [Ca] shoot (%) [Ca] shoot (%) All other taxa Caryophyllales (e.g. sugar beet, carnation)

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

18 Shoot Mg / Ca Ratios in the Caryophyllales 51 species grown hydroponically Plumbaginaceae Polygonaceae Caryophyllaceae Amaranthaceae high 1.2 Aizoaceae Phytolaccaceae Nyctaginaceae low 0 mean Cactaceae Portulacaceae

19 Ecological Implications - Serpentine Flora name is derived from the mineral serpentine ((Mg,Fe) 3 Si 2 O 5 (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,

20 Magnesium : Calcium Ratios in Shoot Tissues Hydroponics Sampled from the field [Mg] shoot (%) 1.0 [Mg] shoot (%) [Ca] shoot (%) [Ca] shoot (%) All other taxa Caryophyllales (e.g. sugar beet, carnation)

21 Magnesium : Calcium Ratios in Shoot Tissues Hydroponics Sampled from the field [Mg] shoot (%) 1.0 [Mg] shoot (%) [Ca] shoot (%) [Ca] shoot (%) All other taxa Caryophyllales (e.g. sugar beet, carnation) Poales (e.g. the grass / cereal family, Poaceae)

22 Magnesium : Calcium Ratios in Shoot Tissues Hydroponics Sampled from the field [Mg] shoot (%) 1.0 [Mg] shoot (%) [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)

23 Magnoliales Laurales Piperales monocots Chloranthales Illiciaceae Schisandraceae Austrobaileyaceae Nymphaceae Amborellaceae Shoot Ca Concentrations of Angiosperm Orders Eudicots > monocots Fagales Cucurbitales Rosales Fabales Oxalidales Malpighiales Celastrales Zygophyllales Myrtales Sapindales Malvales Brassicales Geraniales Saxifragales high 3 % Dipsacales Apiales Asterales Lamiales Solanales Gentianales low 0 Ericales Caryophyllales Proteales Ranunculales

24 Shoot Calcium Concentrations of Monocot Orders high 1.5% Zingiberales Commelinales low 0 Poales Arecales commelinoid monocots Asparagales Dioscoreales noncommelinoid monocots Alismatales shoot Ca concentrations of different monocot orders differ non-commelinoid monocots > commelinoid monocots (Poales, Arecales)

25 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

26 Strontium : Calcium Ratios In Shoots of 44 Plant Species Strontium content (µci/g) Poales Calcium content (mg/g) Andersen AJ (1967) Risö Report 170

27 Phylogenetic Variation in Shoot Mineral Concentrations Proportion of genetic variation Ca Mg Sr order and above (%) within order (%) Ancient evolutionary origin of variation in Ca, Mg & Sr concentrations Broadley et al. (2004) J. Exp. Bot. 55,

28 A Botanical Journey Through The Periodic Table Silicon Hodson et al. (2005) Ann. Bot. 96,

29 % frequency of all observations Silicon in Plants Non-commelinoid monocots (onion) Asterids (daisy) % Si in leaf tissue Hodson et al. (2005) Ann. Bot. 96,

30 % frequency of all observations Silicon in Plants Commelinoid monocots (grass) Non-commelinoid monocots (onion) Asterids (daisy) % Si in leaf tissue Hodson et al. (2005) Ann. Bot. 96,

31 Silicon in Plants Proportion of genetic variation Ca Mg Sr Si order and above (%) within order (%) 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

32 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,

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

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

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

36 Phylogenetic Effects on the Plant Ionome < >2.0 Evolution of Sodium Accumulation in the Caryophyllales

37 Phylogenetic and Environmental Effects on the Plant Ionome Park Grass, Rothamsted

38 Botanical Composition of Park Grass Plots (Crawley et al., ) Crawley et al. (2005) American Naturalist 165,

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

40 Plant Species Differ in Their Ionome 4 Polygonaceae Fabaceae 2 Apiaceae Discriminant Score Poaceae Asteraceae Plantaginaceae Ranunculaceae Discriminant Score 1 White et al. (2012) New Phytologist 196,

41 Calcium : Magnesium Ratios Shoot Mg (mg g -1 DW) Polygonaceae (Caryophyllales) Poaceae other Angiosperm families Shoot Ca (mg g -1 DW) White et al. (2012) New Phytologist 196,

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

43 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, 18 th September 2014

44 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, 18 th September 2014

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